Part 3 - Implants and clinical dentistry
Chapter 1 Implants and periodontology
Field of Periodontology, Graduate School of Medical and Dental Studies,Tokyo Medical and Dental University
Professor Yuichi Izumi
Shinichi Arakawa
Aristeo Atsushi Takasaki
I.

Basic concept for implant

In the 1960s, the Branemark et al. developed osseointegrated implants that function by gaining support
from the bone tissues1). Schroeder et al. later found that that the implants had no ligament tissues
support unlike those of the natural tooth, and that the implant and the bone were in direct binding with
one another2).
The structures of surrounding tissues of implant and natural tooth include: 1. epithelial attachment, 2.
connective fiber tissues and its adherent form, and 3. periodontium. The significant differences that lie
between the surrounding structures of implants and natural teeth are with the latter two factors (2 and
3). The structures of the epithelial attachment (1) for both implant and tooth are similar, however, theepithelial tissues around the implant develop as gingival stratified squamous epithelium in the wound
recovery process. The epithelium of the implant is therefore fundamentally different from those of natural
teeth in terms of developmental studies, and its ability to function as a barrier is reduced. It is also
believed that epithelial layer surrounding implant has fewer barriers function than that of natural teeth.
Many researches regarding roles of implants and soft tissue adhesion in phylaxis have been conducted.
By understanding the differences between the surrounding tissues of implants and those of natural teeth
it should enable the selection of maintenance methods that are most appropriate, and to avoid
inflammation in the surrounding tissues.

A. Structure of periodontal tissue on natural teeth (attachment forms of teeth and ginvivae)
The gingivae consist of mucosal tissues that lie over the alveolar bone and the tooth cervix. The mucosal
tissues consist of three cell layers, epithelial, connective tissue and tunica propria. The characteristicfeatures of this region are the presence of junctional epithelium and oral sulcular epithelium.
The surface of the oral sulcular epithelium is keratinized, and covers the sulcus that lies between theenamel and the free gingiva. The basal cells of the junctional epithelium that lies beneath this are underconstant regeneration. Both basal cells and the cells in the layer above are organized so that the long axis
is parallel to the plane of the tooth.
Connective tissue forms the greater part of the gingivae, and other components are collagen fibers(approx. 60%), fibroblasts (approx 5%), and vessels and nerves (approx 35%). Other cell types include
mast cells, macrophages, and inflammatory cells (including heterophilic leucocytes, lymphocytes andplasma cells). Fiber components are made up primarily of collagen fibers, reticular fibers (in tissues thatlie next to the basal membrane), oxytalan fibers (rare in the gingivae), and elastic fibers (distributed1around the blood vessel sites). With regards to collagen fibers, most of these are in bundles and arearranged in a fixed direction. The gingival fibers can be classified into: a circular group (orientated so as
to encircle the free gingiva), a dentogingival group (spread out in a fan-form in that the fibers extend fromthe root in the cementum at the suprabony pocket, to the buccal and lingual sides or in the direction offree gingiva), a tooth-periosteal group (run from the root in the cementum, past alveolar bone to the sideof the root apex, in the direction of the junctional epithelium), and a transseptal group (run in the
cementum at the suprabony pocket along the side of the tooth) (Fig. 3-1-2).
There are two types of gingival attachments to the teeth, epithelial attachments and connective tissue
attachments. From the alveolar bone to the crown, they are organized in the order of connective tissues,and epithelial attachments, and finally reaching the gingival sulcus. Each is 1 mm wide, a distanceknown as the “biological width” and is a standard that must be taken into account when fabricating theattachments 3).

Fig. 3-1-1
Junctional epithelium andoral

sulcularepithelium

exists in the region of theteeth and gingiva

Fig. 3-1-2
Majority of the collagenfibers are bundled andrun in one direction

Fig. 3-1-3 Epithelial attachment is
an attachment of the epithelial cellswith the teeth. It is attached to theteeth via internal basal lamina andhemidesmosome

B. Structure surrounding the implant body
After implant surgery, mucoadhesion (pierced mucoadhesion) occurs to the implant body protecting theconnective tissues and bone tissues from intraoral substances such as bacteria. The soft tissues
structures surrounding titanium implant abutments have been determined by conducting clinical studies
in human and animal experiments. The research by Berglundh in 1991 conducted on dogs, which has
become the basis for the series of experiments that followed, to compare the biological difference between
the gingivae of natural teeth and the surrounding tissues of the implant body 7). There
were histological similarities between the two. Epithelium of natural tooth gingivae are highly
keratinized and stretch to the junctional epithelium, the main fiber within the subepithelial connective
tissues spread in a fan-shaped form towards the soft and hard tissues surrounding the periodontal2

membrane through the cementum of the tooth root. The mucous membrane around the implant is also
covered by highly keratinized epithelium, which is connected to epithelial barrier facing the abutment.
This epithelial barrier corresponds to the junctional epithelium of natural tooth. The length is roughly 2
mm long and is attached to the surface of implant through hemidesmosome8). However, since implantmaterial is fundamentally a foreign material, the epithelium around the implant is thought to be more
prone to invasion by foreign substances and bacteria than around the natural teeth9).
The collagen fibrils are present within the 1 to 1.5 mm layer of connective tissues that reside in between
the epithelial barrier and alveolar crest. This structure attaches to the plane of the teeth, referred to asconnective tissue adhesion. The difference in the connective tissue attachment between the implantsurroundings and the natural teeth were investigated by Berglundh et al 7).
The cementum exists on the rhizoplane of a natural tooth. The collagen fibers forms bundles on theinterface between the tooth plane and gingivae, and tooth plane and alveolar bone, and run in a lateral
direction to the coronal, and to the root apex. Contrarily, the collagen fibers run from the periosteum of
the alveolar crest, in parallel to the implant surface, or in straight line in bundled form (Fig. 3-1-4-a). The
forms of attachment were analyzed with various implant types by Abrahamasson et al, but a similarpierced mucosal attachment form as mentioned above were found 10).
An analysis of connective tissues constituents in the implant body attachment structures were conductedby Moon et al on dogs. The results showed two types of attachments, where the first did not consist of any
blood vessels with presence of fibroblast that in aligned parallel to the vertical axis of the implant body(collagen 67%, blood vessel/nervous structure 0.3%, fibroblast 32%). The second type was found to exist
external to the former type, that consisted of fewer fibroblast but with higher constitution of collagenfibers and vascular nerve structures (collagen 85%, vasculature 3%, fibroblast 11%).
The investigation into the biological width of the pierced mucosal attachment was also conducted on
dogs12). In this experiment, after implanting into both right and left sides of the jaw, the thickness of theright mucosa was decreased to less than 2 mm. The results showed that the pierced mucosal attachment
to be constructed from 2 mm barrier epithelium and a layer of connective tissue adhesion that was 1 to
1.5 mm thick. In the portion of the mucosa on the right, in which the thickness was decreased, bone
resorption was shown to result in the surrounding ridges of the fixture, and had consequently establisheda thickness of more than 3 mm.
An experiment was conducted to investigate the pocket depth around the implant and the natural toothon beagle dogs13). The probe with 0.5 mm diameter tip was inserted with 0.5 N pressure into clinically
healthy tissues surrounding the implant. The surrounding tissues of implant were pressurized andbecame laterally displaced with the probing. The tip of the probe was inserted to the interface of theconnective tissues and the abutment thus indicting that it was positioned further in than the tip of thebarrier epithelium (Fig. 3-1-4-b). The results showed that the probes became in close contact with thealveolar crest indicating that the soft tissue attachment with the implant surface to be weaker than thoseof the natural teeth. It thus suggested the need to reduce the probing pressure when applying to examine
the implant attachment structures, and in exertion of excess force, there is a risk of mechanically loss of
the attachment between the soft tissues and the implant surface.

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Fig.3-1-4-a

Fig.3-1-4-b
Fig. 3-1-4-a,b
The collagen fibrils in the structures surrounding the implant differ from those of the natural teeth, inthat it starts from the periosteum of the alveolar crest then runs in parallel to the implant surface orlined in a straight line in a bundle form (a). In probing the implant surroundings, the probe tip reaches
further in than the barrier epithelium (b).

II. Its association to periodontal disease
It has been reported that periodontitis and peri-implantitis have many disease states in common.
Peri-implantitis is defined as a loss of the supporting bone caused by inflammation of the tissues
surrounding the osseointergrated implant (Fig. 3-1-5-a, b, c). On the other hand, the fact thatperi-implant mucositis occurs due to accumulation of plaque around the implant and similarly togingivitis, a reversible inflammation of the soft tissue surrounding implant to occur became evident. The
4host responses at the early stages against bacteria are also identical. Peri-implant mucositis also has
common features with periodontitis besides the loss of supporting alveolar bone. Both are induced byperiodontal disease bacteria, and in a similar manner that gingivitis does not always progress toperiodontitis, mucositis does not always progress to periateritis. The distinction however exists between
the two. For periodontitis, the space between the gingivae (existence of bacterial flora) and bone are
separated by the healthy peradentium fibers thus preventing the bacterial infection from directly
affecting the bone. In per-implantitis, however, the infection can directly affect the alveolar bone,
resulting in a lesion.
The causative microorganisms for the peri-implantitis such as, porphyromonas gingivalis, Prevotellaintermedia, Fuso-bacterium spp., and Treponema denticola have been found to be the same as those of
the periodontal disease17) ,18). The causative agent for the periodontal disease present in the periodontal
pocket has been found to easily spread to the tissues surrounding the implant within the oral cavity. The
detection rates of the causative agents for periodontal disease were determined using DNA probes. In
investigating the subgingival periodontal pockets located adjacent to the natural teeth or the implants,
the presence of another unique organism was found known as Tannerella forsythia (Bacteroides

forsythus). This finding indicated that the periodontal pocket serves as a reservoir for microorganisms toreadily spread throughout the mouth, emphasizing the importance of maintaining healthy periodontal
tissues for prevention of the spread of pathogens for implant treatments19).
Monbelli et al. investigated the presence of Gram-positive and Gram-negative bacteria in the samples
collected from the depth of the periodontal pockets and those surrounding the implant of a patient who
was treated for periodontal disease. The analysis of the detection rate of both these bacteria around theimplants, after three or six months, resulted in a positive correlation for both natural teeth and implant
20).

The differences in the flora of the periodontal pockets of the teeth and implant surroudings at the varying
depth within an oral cavity, from the shallow end to the mid-section, were analyzed by Quirynen et al.
using checkerboard DNA-DNA hybridization and real-time PCR. Gram-positive cocci and bacilli,gram-negative bacilli (including periodontal bacteria) and the family of treponema were tested 21). Within
two weeks of the abutment placement, the detection rate for each of the classes including periodontal
disease bacteria, became the same in the area surrounding implant and in the periodontal pocket,
indicating that the bacterial flora to be established in both structures.
The resistance of the tissues to inflammation resulting from the accumulation of plaque is evidently much
lower with the implant than that of natural teeth, with consideration to the nature of the structures
surrounding the implant22). It is therefore essential to treat the periodontal disease of the remaining teeth,
before the osseointegrated-implant treatment to avoid onset of peri-implantitis at the maintenancestages19).

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Fig.3-1-5-a

Fig.3-1-5-b

Fig.3-1-5-c

Fig. 3-1-5-a,b,c
Implantitis is an inflammatory condition arising in the tissues surrounding the implant, giving rise to theloss of the supporting bone.
A. Evaluation criteria for the outcome of implant treatment
Periodontitis is the primary cause of tooth loss; therefore there have been significant number of patients,
affected with periodontitis, who have undergone implant treatment. This has enabled many clinicalexamples to be achieved, and leading to the conclusion of the importance of treating the periodontitis
before the implant treatment. In treating the periodontitis it does not indicate the change in thesensitivity to the pathogens, and whether this will have any consequences on future onsets of implantits;or on the frequency of implant loss is in need of clarification. In other words, the correlation between theperidontitis in the past and the prognosis of implant should be the priority.
A systematic review to investigate of the correlation was conducted by Van der Weijiden et al. in 2005.
Here, the results of implant treatment to periodontis-affected patients and non-peridontitis patients werecompared. The results indicated of the differences in both, the alveolar bone supporting the implant; andin the frequency of implants lost to be the most significant23).
In 2008, Ong et al. also published a systematic review that studied whether periodontal disease in thepast affected the outcomes of implant treatment24), as shown below:
1. Survival rate of implant
Cumulative “survival rate” indicates the existence of implant in the mouth during the observation period;and “unsuccessful rate” indicates the time of losing implant from the time of operation and classify the
number of implant loss.
2. Success rate of implant
The standard for the success of implant had not been defined, therefore Albrektsson et al. Buser et al. andKaroussis et al. made “standard of success” in the cases where the symptoms listed below could not be
detected:
Restlessness. discomfort such as pain, peri-implantitis around implants, acceleration of transparency ofthe bone surrounding implant, existence of pockets with sizes over 5 mm, and more than 0.2 mm progressin mesial or distal perpendicular bone defect after a year25),26),27).
3. State of bone around implant
4. Incidence rate of peri-implantitis
Karoussis et al. defined peri-implatitis as a disease state in which a pocket of size more than 5 mm;presence of bleeding on probing (BOP); and bone resorption to be detected with X-ray radiography28).
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1. Implant survival rate in treated periodontitis compared with non-periodontits patients (Fig. 3-1-6)
The investigations into the implant survival rate in the vast number of studies have employed various
evaluation standards thus making it impossible to draw conclusion from these comparable studies. For
example, the period to be defined from the time of planting the implant or the time that the occlusional
force was applied; or whether each implant or each patient was evaluated as a unit. The unit forevaluation by Karoussis et al., Evian et al., and Roos-Jansåker et al., used of the time of planting theimplant, and Watson et al.and Hardt et al. used the point at which biting force is applied as the standard.
Concerning the evaluating unit, Watson et al., Hardt et al., and Karoussis et al., used each implant,
whereas Evian et al. and Ross-Jansåker et al. used each patient28),29),30),31).
Every other reports except that of Watson et al. showed a good correlation with the survival rate of
implant for patients without a history of peridontitis compared with those treated for periodontitis. Evianet al. and Ross-Jansåker et al. also studied numerous cases for a long duration of time and concluded that
there was a significant difference between the two patient types. However, it was later found that theirobservations were conditional on periodontal states of the patients29),30).

Fig. 3-1-6
Implant survival in treated periodontitis
compared with non-perodontitis patients

2. Implant success rate in treated periodontitis compared with non-periodontitis patients (Fig. 3-1-7)
Similarly, the studies on the success rate of implants varied with their defining factors for evaluationsuch as the time of treatment, either from the time of planting the implant or the time that theocclusional force was applied; or whether to evaluate each implant or each patient as a unit. Thereby it
was impossible to evaluate these results as comparable studies. The unit for evaluation by Rosenberg etal. and Mengel et al., used the time of planting the implant, and Watson et al. used the point at whichbiting force was applied, Brocard et al., used 6 months after the wound healing as the standard, whereas
Karoussis et al. defined the standard as one year, respectively28),31),32,33).
Rosenberg et al. evaluated the failure examples by sorting them into two types. These weredistinguishing by, firstly failure of osseointegration, and secondly, where peri-implantitis resulted32).
Overall, except for the evaluation by Watson’s group, all of the other groups reported differences in the
success rate to exist between the two patient groups. The patients without a past history of periodontitis
had higher success rate than the treated patients. Furthermore, the cohort studies conducted by
Karoussis et al. showed a significant decrease in the success rate of the patients with past history28). With7

regards to the other observations, their significance have not yet been verified.

Fig. 3-1-7
Implant success in treated periodontitis
compared with non-periodontitis patients

3. The state of bone around implants in treated periodontitis compared with non- periodontits patients.
(Fig. 3-1-8)
There have been five volumes of researches reported on the changes in the states of the bones
surrounding implants with X-ray radiography. In all of these studies, the extent of bone resorption inpatients without a history of periodontitis was found to be less than the treated group.
A significant difference was reported by Hardt et al., as an exception. However, since there was no
mentioning of the of the periodontitis treatment that was used, we cannot exclude the possibility that the
progression of periodontal disease could have caused the bone resorption. The publication by Haggi et al.
showed p = 0.058, a borderline, but they have since come to a conclusion that in case of patient withaggressive periodontitis, they are at increased risk of alveolar bone resorption compared with patients
who have not been affected by chronic periodontits or periodontits36). Other researchers have notconducted statistical processing28) to see if there are significant differences in bone resorption33) between
the two patient groups.

Fig. 3-1-8
Bone level change around implants intreatedperiodontitis

compared

with

non-periodontitis patients84. Peri-implantitis around implants in treated periodontitis compared with non-periodontits patients.
Three volumes of thesis28),32),37) indicated the reduction in the frequency of peri-implantitis incidence withimplants in unaffected patient compared with periodontitis treated individuals. Regarding the tworeports published by Karoussis et al. and Ross- Jansåker et al., a significant difference was found between
the two patient groupds. Both researches showed that the patient with a history of periodontitis to havehigher incidence of peri-implantitis and to show low success rate28).

Fig. 3-1-9
Peri-implantitis around implants intrated periodontits compared with
non-periodontitis patients

B. Clinical notes.
Patients who received periodontal treatment are more likely to encounter problems in the areasurrounding the implant, such as loss of implant, bone resorption and inflammation of tissues around theimplant. It is therefore necessary to inform and convince the patients before the implant treatment of thelikeliness of contracting peridontitis later in the course.
The periodontal treatment should be conducted before starting the implant treatment, and by gaining acomprehensive view of the state and the conditions of the surrounding tissues, early detection andtreatment should be possible, preventing the onset of periodontitis and peri-implantitis.

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